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Marbled Salamander

Marbled Salamander

(Murphy, 1962) to hundreds (Graham, with males exhibiting nudging, head- B. Eggs. 1971; Shoop and Doty, 1972; Stenhouse, swinging, lifting, and body-flexing be- i. Egg deposition sites. Breeding sites are 1985a), 1,000 (Pechmann et al., 1991; haviors (Arnold, 1972). Spermatophore generally the dried beds of temporary Semlitsch et al., 1996) to 10,000 (Taylor deposition follows lateral undulations of ponds, the margins of reduced ponds, or and Scott, 1997). However, given the re- the tail. Spermatophores are 4–5.5 mm tall dry floodplain pools. Female marbled liance of marbled on small (Lantz, 1930; illustrated in Noble and salamanders construct nests and lay eggs isolated seasonal wetlands and intact Brady, 1933). Typical and secondary sper- under virtually any cover in situations forested floodplain habitats, their abun- matophore deposition may occur (Arnold, where the nest is likely to be flooded by dance presumably has declined as wetland 1972, 1976; personal observation); a male subsequent winter rains (Noble and Brady, habitats have been destroyed (Petranka, may deposit over 10 spermatophores in 1933). Eggs are laid on the edges of pools 1998). For example, from the 1950s–70s 30–45 min (L. Houck, personal communi- (Dunn, 1917b) and in dry basins under the loss of wetlands in the Southeast was cation). Males will mate with females vegetation ( Jackson et al., 1989), logs greater than in any other region of the outside what is typically thought of as (Bishop, 1924; Doody, 1996), and leaf de- country, with a net annual loss of 386,000 the wetland margin (Krenz and Scott, bris (Deckert, 1916; Petranka and Petranka, ac/yr (Hefner and Brown, 1985); in North 1994). Males often will court other males 1981b). Eggs are laid occasionally on non- Carolina approximately 51% of all wet- (Noble and Brady, 1933), including sper- soil substrate (Brimley, 1920a). Nest site land acreage on the Coastal Plain has matophore deposition in the absence of a selection by females is influenced by mi- been lost (Richardson, 1991), including female (L. Houck, personal communica- crosite elevation within the pond bed, 70% of the pocosins that have been “de- tion). Females may follow a male to pick site hydrologic regime, cover availability, veloped” or partially altered (Richardson, up a spermatophore (Noble and Brady, and soil moisture (Petranka and Petranka, 1983); approximately 97% of the Carolina 1933) or simply move about an area until 1981a,b; Jackson et al., 1989; Figiel and bays on the Coastal Plain of South Carolina a spermatophore is located (Arnold, Semlitsch, 1995; Wojnowski, 2000; but have been altered or severely impacted; 1972). When a spermatophore contacts a see also Marangio and Anderson, 1977). and 200 bays of the original thousands female’s vent she will lower herself onto it Females actively excavate oblong to ovoid- are “relatively unimpacted” (Bennett and and insert it into her cloaca (Arnold, shaped depressions (King, 1935; Petranka Nelson, 1991). 1972). Sperm are stored in exocrine glands and Petranka, 1981b). called spermathecae in the roof of the ii. Clutch size. Of the three reproductive 3. Life History Features. cloaca (Sever and Kloepfer, 1993). Eggs are modes of salamanders outlined by Salthe A. Breeding. Reproduction is terrestrial, fertilized internally by sperm released (1969), marbled salamanders have an in or near the wetland breeding sites prior from spermathecae during oviposition atypical type I mode (Salthe and Mecham, to pond filling. (Sever et al., 1995). Females may pick up 1974; Kaplan and Salthe, 1979). Clutch size i. Breeding migrations. Onset of breeding multiple spermatophores (Arnold, 1972), ranges from approximately 30 to 200 migrations occurs from September–No- but sperm competition has not been de- eggs (see Petranka, 1998) and usually is vember. Timing varies geographically and finitively demonstrated. Sperm in the positively correlated with female body may occur 1 mo or more earlier at south- spermathecae do not persist for 6 mo size (Kaplan and Salthe, 1979; Walls and ern latitudes compared with northern lat- after oviposition (Sever et al., 1995). Males Altig, 1986; Petranka, 1990; Scott and Fore, itudes (Anderson and Williamson, 1973). will mate with females beyond what hu- 1995), although not always (Kaplan and On a broad scale, seasonal migrations are mans typically define as the wetland mar- Salthe, 1979)—larger females may have probably linked to regional climatic and gin (Krenz and Scott, 1994). larger eggs (Kaplan and Salthe, 1979). hydrological cycles (Salthe and Mecham, ii. Breeding habitat. Marbled salaman- Compared to other of Am- 1974). Adult salamanders move to breed- ders are one of two species of Ambystoma bystoma, females in some populations of ing sites on rainy nights and tend to enter that breed on land (Petranka, 1998), and marbled salamanders may have fewer, and exit the site at approximately the they are the only Ambystoma species that larger eggs than would be expected for an same point (Shoop and Doty, 1972; P.K. exhibit parental care (Nussbaum, 1985, of their size (Kaplan and Salthe, Williams, 1973; Douglas and Monroe, 1987). Due to the terrestrial reproductive 1979; D.E.S., unpublished data; for a dif- 1981; Stenhouse, 1985a). Males generally habits of marbled salamanders, breeding ferent opinion see Nussbaum, 1985, 1987). arrive at the breeding site before females is restricted to fish-free wetlands with sea- For example, comparing female marbled (Noble and Brady, 1933; Graham, 1971; sonally fluctuating water levels that in- salamanders and mole salamanders (A. Krenz and Scott, 1994). In a 25-yr study at clude upland hardwood “swamp forests” talpoideum) of equal body size, marbled Rainbow Bay in South Carolina (see Seml- (King, 1935), bottomland hardwood pools salamanders have 3–4 times fewer eggs, itsch et al., 1996), the mean date of arrival (Viosca, 1924a; Petranka and Petranka, but each egg is 3–4 times larger with 3–4 of males at the breeding site was 10 d ear- 1981a,b), quarries (Graham, 1971), vernal times higher lipid amounts (Komoroski, lier than females (unpublished data), per- ponds (Doty, 1978), Carolina bays ( Jack- 1996; D.E.S., unpublished data). Mean haps due solely to the combination of a son et al., 1989; Gibbons and Semlitsch, egg diameter is greater in marbled sala- limited number of nights suitable for mi- 1991), and floodplain pools (Petranka, manders than in flatwoods salaman- gration and slower nightly movements by 1990). Females remain with eggs (Noble ders (A. cingulatum; 2.8 vs. 2.3. mm; fat, gravid females (Blanchard, 1930; per- and Brady, 1933) for varied lengths of Anderson and Williamson, 1976). Mean egg sonal observations). The sex ratio of the time (Petranka, 1998); they may leave be- dry mass is greater in marbled salaman- breeding population is often biased to- fore eggs are inundated (McAtee, 1933; ders than in either mole salamanders ward males (Graham, 1971; Stenhouse, Jackson et al., 1989; Petranka, 1990). Nest or spotted salamanders (A. maculatum; 1987; Krenz and Scott, 1994), in part be- brooding appears to enhance embryonic Komoroski, 1996). The caloric content cause males mature at an earlier age survival (Petranka and Petranka, 1981b; (cal/mg dry mass) of marbled (Scott, 1994; Pechmann, 1994). The sex Jackson et al., 1989), although the mecha- eggs is greater than the energy content of ratio in one study (Parmelee, 1993) during nism is unknown. Opinions differ on spotted salamanders and tiger salamander the non-breeding season did not differ whether there is an energetic cost to (A. tigrinum) eggs (Kaplan, 1980b). Rela- from 1:1. brooding by females (Kaplan and Crump, tively few, large eggs with lipid stores in a. Courtship activity. At the time of au- 1978; versus D.E.S., unpublished data). excess of the amount needed for embryo- tumn migration, males are at maximal Occasionally nests are communal (Gra- genesis probably reflects a response to the testosterone levels (Houck et al., 1996; un- ham, 1971; Petranka, 1990), especially if terrestrial breeding habits of marbled sala- published data). Courtship is terrestrial, cover items are scarce (Palis, 1996b). manders and the extreme variability and

628 unpredictability in the timing of hatching 1996; table 1), depending upon their den- 1970). Larvae nearing metamorphosis re- (i.e., the duration of the egg stage). Sub- sity, food levels, and temperature. Growth main near the bottom at night (Petranka stantial (15–30%) variation in egg diame- rates are comparable to spotted salaman- and Petranka, 1980). ter occurs within and among populations ders (Walls and Altig, 1986), but compar- iii. Larval polymorphisms. None reported, (Kaplan, 1980a). Egg size is positively isons to mole salamanders differ (Keen et although behavior differences are known. correlated with hatchling size and early al., 1984; Walls and Altig, 1986). Although Laboratory assays have demonstrated two larval size (Kaplan, 1980a). larval growth is temperature dependent divergent aspects of kin recognition. In In spite of terrestrial egg laying, egg (Stewart, 1956), temperature effects may some contexts, kin recognition may reduce structure in marbled salamanders is simi- not be as pronounced as in some other aggression and cannibalism among sib- lar to aquatic Ambystoma species (Salthe, Ambystoma species (Keen et al., 1984). lings in larval marbled salamanders (Walls 1963). Egg development is temperature- Food level, temperature, hatching time, and Roudebush, 1991); whereas in other dependent (Noble and Brady, 1933); de- and larval density affect traits of newly contexts, large larvae may eat siblings velopment (at similar temperatures) is metamorphosed (Stewart, 1956; preferentially (Walls and Blaustein, 1995). slower than for some other ambystom- Boone et al., 2002). Early hatching larvae Hokit et al. (1996) further demonstrated atids (Moore, 1939). The prospective neu- are larger at metamorphosis, have higher that kin discrimination is context depend- ral tissue of marbled salamanders has a survival, and metamorphose earlier than ent. Under more natural conditions, kin- lower density and higher water-holding late-hatching larvae (Boone et al., 2002). ship effects on larval performance did not capacity than the embryonic tissue of Higher food levels and warmer tempera- occur (Walls and Blaustein, 1994). aquatic breeders such as spotted salaman- ture promote earlier metamorphosis; in- iv. Features of metamorphosis. As noted ders and tiger salamanders (M.G. Brown, creased prey density promotes larger size above, at high larval densities individual 1942). Embryos develop to a hatching at metamorphosis (Stewart, 1956). Early- larvae have slower growth, a smaller size stage, but do not hatch until stimulated hatching larvae are larger at metamorphosis, at metamorphosis, and reduced survival by hypoxia when the nest is flooded (Pe- have higher survival, and metamorphose (Petranka, 1989c); they may also have tranka et al., 1982). Some eggs may remain earlier than late-hatching larvae (Boone longer larval periods (Scott, 1990). In field viable several months after oviposition et al., 2002). Intraspecific larval density experiments, environmental conditions (Noble and Brady, 1933), but often eggs affects larval growth and a suite of larval (i.e., larval density) accounted for more of laid in October will die by December if traits (Stenhouse et al., 1983; Stenhouse, the variation in body size at metamor- the nest has not been flooded (McAtee, 1985b; Smith, 1988, 1990; Petranka, 1989c; phosis than did an individual’s level of 1933). An embryo’s lipid reserves in Scott, 1990). At high densities, larvae have multilocus genetic heterozygosity (Chazal excess of reserves required for embryo- slower growth, smaller size at metamorpho- et al., 1996). In an artificial pond study, genesis constrain the maximum time an sis, and reduced survival (Petranka, 1989c); more heterozygous individuals had shorter embryo can survive in the egg (unpub- they may also have longer larval periods larval periods than did less heterozy- lished data). Hatching under natural (Scott, 1990). As ponds dry, larval densities gous larvae (Krenz, 1995). Juvenile recruit- conditions may occur at a wide range of may become extremely high (e.g., 237 m2; ment into the terrestrial population may developmental stages (Noble and Brady, Smith, 1988). vary dramatically among sites and years 1933; Graham, 1971), probably due to ii. Larval requirements. (Stenhouse, 1984, 1987; Pechmann et al., the hydration state during development a. Food. Larvae eat primarily macro- 1991; Taylor and Scott, 1997), which and the timing of nest inundation (Noble zooplankton, beginning with copepod probably reflects broad variation in abi- and Brady, 1933; S. Dooty, personal com- nauplii in hatchlings (Petranka and Pe- otic (e.g., hydroperiod) and biotic (e.g., munication). Larvae will hatch from early tranka, 1980). Ostracod, cladoceran, and productivity, competition, and predation) stages (10.5 mm), with much yolk and copepod zooplankton feed larger larvae. conditions (Petranka, 1989c; Semlitsch little swimming ability, to late stages (20 mm; Other invertebrate prey include chirono- et al., 1996). Effects initiated by aquatic Brimley, 1920a; McAtee, 1933; Noble and mids, amphipods, chaoborids, and isopods conditions persist in terrestrial adults Brady, 1933). By 18 mm the balancers (Petranka and Petranka, 1980; Branch and (Scott, 1994). are usually lost whether or not the egg Altig, 1981). Timing of metamorphosis may vary has hatched (Brandon, 1961). Embryo b. Cover. Larvae may remain mostly geographically, although recently meta- mortality can be high due to freezing, hidden on the pond bottom during the morphosed juveniles generally disperse dehydration, predation, or fungus (Sten- day and move into the water column at from the breeding site in late spring. house, 1987; Jackson et al., 1989) and is night (Anderson and Graham, 1967; Pe- Metamorphosis occurred in June–July in dependent on the timing and extent of tranka and Petranka, 1980; Branch and (Smith, 1961); June in New York pond-filling. Altig, 1981). Both the limited diurnal (Bishop, 1941b); late May to early June Timing of hatching varies among sites movements and increased nocturnal ac- in Maryland (Worthington, 1968), New and years (Petranka and Petranka, 1980). tivity may serve to enhance feeding and Jersey (Hassinger et al., 1970), and north Within a site, pond-filling may be incre- avoid vertebrate predation (Hassinger et Georgia (Martof, 1955); mid-May in mental or sudden; gradual pond-filling al., 1970; Branch and Altig, 1981), al- West (Green, 1955); mid-April may result in staggered hatching of eggs though larvae floating in the water col- to May in North Carolina (Stewart, 1956; and substantial size variation of larvae umn at night did not capture more prey Smith, 1988); March–April in Alabama within a pond (Smith, 1988). than those feeding on benthos during (Petranka and Petranka, 1980); and as C. Larvae/Metamorphosis. daylight (Petranka and Petranka, 1980). early as mid-March in Louisiana (Dundee i. Length of larval stage. Hatchling densi- Movements of larvae into the water col- and Rossman, 1989). Although marbled ties average as high as 47 larvae/m2 umn are associated with decreased light salamanders will metamorphose in re- (Smith, 1988). Catastrophic larval mortal- intensity (Hassinger and Anderson, 1970) sponse to pond drying, timing also ap- ity may result from winter kill due to ex- as well as vertical stratification of some pears to be triggered by intrinsic factors treme cold (Heyer, 1979; Cortwright and prey species (Anderson and Graham, (Hassinger et al., 1970; Scott, 1994). Lar- Nelson, 1990), incomplete pond filling 1967; Petranka and Petranka, 1980). Lar- vae that hatch 2–3 mo later than others and subsequent drying (King, 1935; Pe- val activity may also vary seasonally; lar- will nonetheless metamorphose within a tranka and Petranka, 1981a), and early vae remain near the bottom of the water few weeks of early hatching larvae, but at pond drying (Pechmann et al., 1991). column early in the season and utilize the a smaller body size (unpublished data). Larval growth rates of marbled sala- entire column for feeding on zooplankton Stages of metamorphosis are described by manders vary considerably (see Doody, as the season progresses (Hassinger et al., Grant (1931).

AMBYSTOMATIDAE 629 v. Post-metamorphic migrations. Juveniles bled salamanders (n 8) by using radioac- i. Heat stress. Larvae of marbled sala- may not disperse far from the edge of wet- tive wire tags. The spring and summer manders have less resistance to high lands (P.K. Williams, 1973) and therefore home range size varied from 1–225 m2, temperatures (i.e., have a lower Critical require intact terrestrial habitats surround- with a median of 14.5 m2. There was a ten- Thermal Maximum, CTM) than either ing the breeding sites (Semlitsch, 1998). dency for home range size to increase as small-mouthed salamanders or spotted vi. Neoteny. There are no reports of non- individuals were followed for longer peri- salamanders (Keen and Schroeder, 1975). transforming marbled salamanders. Given ods. A laboratory study indicated that ju- Smaller adult salamanders reach their CTM the widespread distribution and numerous venile marbled salamanders tend to stay faster than larger adults (Hutchison, 1961). population studies on this species, it is un- on their own marked substrate, which The possible relationship between CTM in likely that neotenic adults exist. may be a mechanism to detect home areas eggs, larvae, and adults, and geographic D. Juvenile Habitat. Same as adult by chemical cues (Smyers et al., 2001). distribution or timing of breeding (sensu habitat, although juveniles tend to occur G. Territories. Although Martin et al. Gatz, 1971) is unknown. under smaller cover objects (Parmelee, (1986) found no evidence for territorial- ii. Water stress. In general, post-meta- 1993). Juveniles retain the ability to dis- ity in small-mouthed salamanders (A. morphic marbled salamanders do not criminate their siblings, presumably by texanum), they suggested that territorial- appear to respond well to prolonged im- chemoreception, for 8 mo after meta- ity might be expected in marbled sala- mersion in water (personal observation). morphosis (Walls, 1991). Juvenile mar- manders. Individuals of some Ambystoma Interestingly, the total oxygen uptake bled salamanders experienced low first- species may return to their summer home through pulmonary surfaces is relatively year survival (4.5%) in old field terrestrial range from the previous year (Semlitsch, low (34%; Whitford and Hutchison, 1966b), enclosures when compared to survival in 1983b), and this may be true in marbled although lung sacs, ridges, and vascular- forest enclosures (45%; Rothermel, 2003). salamanders (P.K. Williams, 1973). The ization are well developed in marbled sala- Juveniles 1 yr old experienced near zero orientation behavior exhibited by mar- manders (Czopek, 1962). Under anoxic annual survivorship in old field enclo- bled salamanders is a necessary precursor conditions, larvae may exhibit anaerobic sures compared to 70% in forest enclo- to territoriality, although territoriality it- glycolysis (Weigmann and Altig, 1975). sures (Rothermel, 2003). self has not been documented. In labora- iii. Metabolic rate. Lunged salamanders, E. Adult Habitat. Most reports of terres- tory studies, “resident” individuals tend including marbled salamanders, increase trial habitats indicate that mature decidu- to bite conspecific “intruders;” however, levels of oxygen consumption with in- ous forests are preferred (Petranka, 1998). animals housed together for long periods creasing body size (Whitford and Hutchi- Mixed hardwood and pine stands (Smith, did not avoid each other (Ducey, 1989). son, 1967; Krenz, 1995). A daily cycle also 1988; Pechmann et al., 1991), floodplains Juvenile salamanders (8 mo old) are less occurs, with resting metabolic rate in- (Petranka, 1989c; Parmelee, 1993), and aggressive to familiar “neighbors” than to creasing by 50% during the early evening uplands (Smith, 1961) are also utilized. unfamiliar “strangers,” especially among (Krenz, 1995). Metabolic rates increase by Of 15 radioactively tagged individuals siblings (Walls, 1991). Adult marbled sala- 119% following dehydration (Sherman released near a woodland pond in southern manders maintained on a low-food diet and Stadlen, 1986). Resting metabolic rate , 14 were tracked in hardwood for- were more prone to bite an intruding sala- is positively correlated with multi-locus est, 1 in an old field (P.K. Williams, 1973). mander than those on a high-food diet heterozygosity (Krenz, 1995); more het- Microhabitats within the forest include (Ducey and Heuer, 1991), which may in- erozygous females with higher metabolic under leaf litter and small mammal bur- dicate that aggression functions to repel demands allocated less energy to their rows (P.K. Williams, 1973; Douglas and an intruder from an individual’s feeding clutches of eggs (Krenz, 1995). Monroe, 1981). Salamanders do not ac- area/burrow refuge. Marbled salamanders I. Seasonal Migrations. Restricted to tively dig their own burrows, but enlarge almost always occur alone under cover ob- times of breeding (adults; see “Breed- existing openings (Semlitsch, 1983a). Al- jects (Parmelee, 1993). ing migrations” above) and following though generally described as woodland H. Aestivation/Avoiding Desiccation. metamorphosis (juvenile; see “Features of salamanders, marbled salamanders may Marbled salamanders likely undergo pro- metamorphosis” above). Post-metamorphic also be tolerant of relatively dry condi- longed periods of summer inactivity, dispersal is restricted to rainy nights. The tions (Cagle, 1942; Smith, 1961; Mount, corresponding to periods of little or no period between metamorphosis and disper- 1975; Dundee and Rossman, 1989) and rainfall. Despite reports that marbled sal may be several weeks or more (depend- can be found on rocky hillsides ( Johnson, salamanders can occur in unusually dry ing on occurrence of nighttime rainfall) 1987). One laboratory experiment indi- habitats (e.g., Bishop, 1943), there is no and is likely a period of high mortality for cated a preference for relatively basic sub- evidence that they differ from more juveniles (personal observation). strates (pH 7.7), although animals in the aquatic species in terms of their water ex- J. Torpor (Hibernation). In the north, field were found on more acidic (pH 5.5) change with soil (Spight, 1967b). How- post-reproductive adult marbled salaman- substrates (Mushinsky, 1975). Compared ever, a laboratory study of water loss rate ders move 30 m from the breeding site to other ambystomatids, marbled sala- showed marbled salamanders lose water (Douglas and Monroe, 1981), where manders may use substantially drier more slowly than the other species exam- they remain for the winter. Hibernation habitat and tolerate higher substrate ined (which were all plethodontids) and in the southern portions of their range is temperatures (Parmelee, 1993). Adults dis- were able to withstand dehydration unknown. persed an average of 194 m from the wet- 30% of initial body weight (Spight, 1968). K. Interspecific Associations/Exclusions. land breeding site (P.K. Williams, 1973). Dehydrated salamanders incur substan- Due to the terrestrial breeding habits and Consequently, post-metamorphic indi- tial metabolic costs, however (Sherman early egg hatching, larval marbled sala- viduals require intact terrestrial habitats and Stadlen, 1986). To minimize water manders are often much larger than other surrounding the breeding sites (Semlitsch, loss, marbled salamanders likely avoid larvae (Worthington, 1968, 1998). Survivorship of marbled salaman- desiccating conditions; as soils dry in 1969; Keen, 1975; Stenhouse et al., 1983; der adults and recently metamorphosed late summer, animals may retreat to Walls and Altig, 1986; Smith, 1988; Scott, 2 animals was low in 100 m enclosures in deeper burrows (P.K. Williams, 1973). 1993). Larval marbled salamanders will clearcuts compared to enclosures in ad- Rehydration rates were faster in marbled feed on other amphibian eggs and larvae jacent forests (P. Niewiarowski and A. salamanders than in more aquatic species, (Walters, 1975), including Ambystoma lar- Chazal, personal communication). and faster in severely dehydrated ani- vae. Where they co-occur, marbled sala- F. Home Range Size. Williams (P.K., mals than in less-dehydrated individuals manders eat smaller spotted salamander 1973) examined home range size for mar- (Spight, 1967a). larvae (Stewart, 1956; Stenhouse et al.,

630 AMBYSTOMATIDAE 1983; Stenhouse, 1985b), small-mouthed N. Feeding Behavior. Stomach contents exhibit tail lashing, body coiling, and salamanders (Walters, 1975; Doody, 1996), of juveniles and adults include millipedes, head-butting behaviors, and/or may be- Jefferson salamanders (A. jeffersonianum; centipedes, spiders, insects, and snails come immobile (Brodie, 1977). Such be- Cortwright, 1988), tiger salamanders (Dundee and Rossman, 1989); , haviors may draw the attacks toward the (Stine et al., 1954), and mole salaman- annelids, and mollusks (Smith, 1961). tail, which has concentrations of granular ders (Walls, 1995). Spotted salamander O. Predators. glands on dorsum that produce noxious larvae may be more susceptible than i. Eggs. Eggs may be preyed upon by secretions. Adults are unpalatable to com- larvae to this predation beetles, salamanders, frogs (Noble and mon ribbon snakes (T. s. sauritus; T. Mills, due to increased use of refugia by mole Brady, 1933), and possibly a millipede personal communication). Secretions salamanders (Walls, 1995). The size of species (Uroblaniulus jerseyi; Mitchell et al., generally confer protection from a single marbled salamander larvae at the time 1996a). attack by shrews (Brodie et al., 1979). Se- when other Ambystoma eggs are hatching ii. Larvae. Larvae are palatable to fishes cretions in marbled salamanders are re- varies among ponds and years by 30–40% (Kats et al., 1988), but usually do not in- duced after multiple attacks by shrews, (Stenhouse et al., 1983). Consequently, al- habit ponds where fish occur. Larval mar- resulting in increased vulnerability (Di- though larval marbled salamanders are bled salamanders are prey for numerous Giovanni and Brodie, 1981). often predators, they may also be com- species, especially invertebrates includ- Q. Diseases. An aquatic fungus (Sapro- petitors (Wilbur, 1984; Stenhouse, 1985b; ing dragonfly naiads (Odonata), spiders legnia sp.) may develop on the injured Cortwright, 1988; Semlitsch et al., 1996). (Arachnida), dytiscid beetle larvae and portions, especially limbs, of bitten larvae Predation by marbled salamander larvae adults (Coleoptera), and giant water bugs and may be lethal (Petranka, 1989c). may substantially affect community dy- (Bellostomatidae). Larval survivorship Marbled salamanders have been used namics (Cortwright and Nelson, 1990; decreased from 60 to 70% to 20% when in toxicological tests of hydrazine com- Morin, 1995; Boone et al., 2002). Juvenile hatchlings inhabited experimental en- pounds (Slonim, 1986), beryllium sulfate marbled salamanders that were tested closures in a wetland replete with in- (Slonim and Ray, 1975), pesticides (Hall under laboratory conditions with con- vertebrate predators (unpublished data); and Swineford, 1981), and motor oil (Lef- specifics and with juvenile mole salaman- survivorship decreased to zero in a year court et al., 1997). ders did not show any overt aggression, when chain pickerel (Esox niger) colonized R. Parasites. Rankin (1937) reported perhaps indicating that such behavioral the wetland. Adult eastern newts (Notoph- the following parasites from marbled interactions are not important for juve- thalmus viridescens) and paedomorphic salamander larvae in North Carolina: niles (Smyers et al., 2001). Additional mole salamanders also feed on larval mar- Protozoa—Cryptobia borreli, Eutrichomas- experiments with juvenile spotted sala- bled salamanders. Cannibalism may occur tix batrachorum, Hexamitus intestinalis, manders indicated that juvenile marbled (Walls and Roudebush, 1991) when incre- Prowazekella longifilis, Tritrichomonas au- salamanders may defend burrow space by mental pond-filling staggers dates of gusta; Trematoda—Diplostomulum am excluding heterospecific salamanders hatching and increases size variation bystomae; Acanthocephala—Acantho- (Smyers et al., 2002). (Smith, 1990). Wading birds and kingfish- cephalus acutulus. Rankin (1933) reported L. Age/Size at Reproductive Maturity. ers (Megacerle alcyon) are also likely preda- the following parasites from marbled sala- Age and size at reproductive maturity are tors (personal observations). mander adults in the same populations: traits that vary and are highly dependent iii. Juveniles and adults. Raccoons (Pro- Protozoa—Cryptobia borreli, Cytamoeba on size at metamorphosis (Scott, 1994), cyon lotor), opossums (Didelphis virgini- bacterifera, Eimeria ranarum, Eutrichomas- which in turn is influenced by intraspe- ana), skunks (Mustelidae), and shrews tix batrachorum, Haptophyra michiganensis, cific larval densities and the timing of (Soricidae) are known to kill adult mar- Hexamastix batrachorum, Hexamitus intesti- pond drying (Petranka, 1989c; Scott, bled salamanders (DiGiovanni and Brodie, nalis, Prowazekella longifilis, Tritrichomonas 1990). Males tend to mature at an earlier 1981; Petranka, 1998). Often the tails are augusta; Trematoda—Brachycoelium hospi- age than females (Scott, 1994; Pechmann, not eaten (personal observation). Newly tale, Diplostomulum ambystomae; Gorgode- 1995); average age at first reproduction for metamorphosed animals may be sus- rina bilobata, Megalodiscus temperatus, males is 2.5–3.1 yr (Scott, 1994) to 3.3 yr ceptible to mammalian predators as Plagitura sp.; Nematoda—Capillaria in- (Pechmann, 1995), and for females, 2.8– well as some snakes; one southern water equalis, Cosmocercoides dukae, Filaria sp., 3.4 yr (Scott, 1994) to 4.0 yr (Pechmann, snake (Nerodia fasciata) had eaten 34 spirurid cysts; Acarina—Hannemania dunni. 1995). The range of age at first reproduc- recently metamorphosed marbled sala- The trematode Brachycoelium am- tion for both sexes is 1–7 yr. Mean size at manders (unpublished data). Liner (1954) bystomae was reported from marbled first reproduction is approximately 53–60 reported ingestion of two recently salamanders by Couch (1966), and an mm SVL for both sexes (Scott, 1994; Pech- metamorphosed marbled salamanders unidentified immature trematode by Male- mann, 1995); the minimum size at first re- by a western ribbon snake (Thamnophis witz (1956). The gall bladder myxosporean production may be smaller for males proximus). (Myxidium serotinum) has been reported (42.0 mm) than for females (45.0 mm). P. Anti-Predator Mechanisms. in marbled salamanders in Arkansas and M. Longevity. Survival to first reproduc- i. Eggs. Protection of eggs from preda- (McAllister and Trauth, 1995). tion can be low and is influenced by size at tors is possibly one function of nest- metamorphosis. Variation in body size at brooding by females (Petranka, 1990). 4. Conservation. metamorphosis is coupled with variation ii. Larvae. Limited diurnal movements Marbled salamanders are listed as Threat- in lipid stores (ranging from 2–16.5% of and hiding in benthic debris may reduce ened in Massachusetts and Michigan, dry mass; unpublished data). Small, lean predation (Hassinger et al., 1970; Petranka and Protected in New Jersey (Levell, 1997). animals may suffer the highest mortality and Petranka, 1980; but see Marangio, In each of these states, permits are re- immediately following metamorphosis 1975, for report of positive phototaxis in quired for any activity involving marbled (Scott, 1994). Survival from metamorphosis small larvae). Hatchlings and small larvae salamanders. to first reproduction ranges from 3–60% may use the sun as a cue to orient toward Given the reliance of marbled sala- (Scott, 1994; Pechmann, 1994, 1995). Males deep water (Tomson and Ferguson, 1972). manders on small isolated seasonal wet- may exhibit higher survivorship than fe- Larvae do not change behavior (i.e., in- lands and intact forested floodplain males due to their earlier age at first repro- crease use of refugia) in the presence of habitats, their abundance presumably has duction (Scott, 1994). Maximum lifespan fishes (Kats et al., 1988). declined as wetland habitats have been in the field appears to be 8–10 yr (Graham, iii. Adults. Animals under attack by destroyed (Petranka, 1998). Small isolated 1971; Taylor and Scott, 1997). short-tailed shrews (Blarina brevicauda) wetlands are the most valuable wetlands

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